J.C.M. Trail and G.D. M. d'IETEREN1
SUMMARY
Considerable progress has been made in defining and measuring criteria of trypanotolerance since the late 1970's, when ILCA, FAO and UNEP worked with researchers in 18 West and Central African countries to show clear relationships between level of trypanosomiasis risk and animal performance. During 1980's, work with N'Dama cattle at sites of the African Trypanotolerant Livestock Network quantified the effects of ability to control the development of anaemia on a number of cattle performance traits. Results showed that packed red cell volume (PCV) values when parasitaemic were closely related to animal performance, and could be measured satisfactorily in one-year-old calves. AS PCV values had higher heritabilities than, and positive genetic correlations with, growth, there appeared to be definite possibilities for selection of trypanotolerant animals on the basis of control of anaemia development.
In contrast during the 1980's, the degree of parasitaemia could not be so accurately quantified using the buffy coat technique available for field use. So, in 1990 antigen-detection enzyme immunoassays (antigen-ELISA) developed at the International Laboratory for Research on Animal Diseases were utilized. Early results showed that the antigen-ELISA is significantly more sensitive in monitoring Trypanosoma congolense and T. vivax infections and has the potential to increase the efficacy of selection of trypanotolerant N'Dama cattle under tsetse challenge in the field in three main ways.
1 International Livestock Centre for Africa (ILCA), Nairobi, Kenya.
Accurate identification of trypanosome species, especially in mixed species infections, clarifies relationships between infection, anaemia and animal performance.
Detection of animals antigenaemic without patent parasitaemia could allow individuals with superior ability to control trypanosome infection to be identified.
More accurate measurement of the proportion of time an animal is infected allows more accurate evaluation of its anaemia control capability.
I. BACKGROUND
Much consideration is being given to the use of breeds of domestic animals that possess the ability to survive and be productive in tsetse-infested areas without the aid of trypanocidal drugs. This trait has been termed trypanotolerance and is generally attributed to N'Dama and West African Shorthorn cattle as well as to their sheep and goat counterparts. Major constraints to putting genetic resistance to trypanosomiasis to practical use have been related to difficulties in the definition and measurement of criteria of trypanotolerance. We believe this to be an appropriate time to review the subject, as considerable progress has been made since the late 1970's when ILCA, FAO and UNEP worked with researchers in 18 West and Central African countries to build up general relationships between trypanosomiasis risk and animal performance. They used all available information from the many individual projects that had previously been undertaken in these countries (ILCA/FAO/UNEP, 1979).
Most work following on in the 1980's was carried out on the N'Dama breed, the most important of the trypanotolerant cattle breeds. Much was accomplished within the African Trypanotolerant Livestock Network, by National Researchers in many West and Central African countries. This clearly indicated that ability to control the level of parasitaemia and to control the development of anaemia are key indicators of the trypanotolerance trait, and that these processes, although controlled genetically, are not necessarily linked to each other (most recently reviewed by Murray, et.al., 1990).
In field studies, the degree of anaemia can be easily quantified by measuring packed red cell volume percent (PCV). This has allowed progress to be made in relating control of anaemia development to animal productivity (Trail et al., 1991b); in evaluating a field test for anaemia control in young N'Dama cattle to help in choosing replacement animals (Trail et al, 1991a); and in investigating the possibilities of genetic selection for trypanotolerance based on PCV measurements (Trail et al., 1991c). In contrast, the degree of parasitaemia is not so easily quantified, and has depended on demonstration of trypanosomes in peripheral blood by parasitological techniques. The most sensitive practical field approach has been to detect the presence of trypanosomes by the dark ground/phase contrast buffy coat method (Murray et al., 1977)) and quantify the intensity of the infection as a parasitaemia score (Paris et al., 1982). However, a high proportion of infections go undetected as many infections are chronic, fluctuate markedly and may be below the limit of detection of this technique. Thus at the end of the 1980's it seemed possible to plan improvement programmes based on the anaemia control component as measured by PCV when infected, but not on actual infection data as measured by the buffy coat technique.
So, in 1990, field work started using recently developed antigen-detection enzyme immunoassays (antigen-ELISA) for the diagnosis of Trypanosoma vivax, T. congolense and T. brucei infections (Nantulya and Lindqvist, 1989, Nantulya, 1990). The assays are based on monoclonal antibodies which recognise trypanosome antigens specific for the three trypanosome species. the antigen-ELISA has been shown to be four times more sensitive than the buffy coat technique in monitoring T. congolense infection in cattle (Masake and Nantulya, 1991). This is because the buffy coat technique detects only trypanosomes present in the peripheral blood circulation. The number of trypanosomes is often too small in chronic infections for detection by this technique, despite the fact that there may be many trypanosomes in other body organs such as the spleen, liver and lymph nodes. The antigen-ELISA, on the other hand, detects soluble antigens released by dying trypanosomes wherever they may be. The sensitivity of this test, thus, does not depend upon parasite numbers in peripheral circulation; hence the high sensitivity even when there may be no detectable parasitaemia. Results from this recent and still very much ongoing work (Trail et al., in press; Trail et al., submitted), indicate that antigen-ELISA has potential to greatly increase the efficiency of selection of trypanotolerant N'Dama cattle under tsetse challenge in the field.
This paper focuses on these aspects of, and relationships between, trypanosome infection, anaemia control and performance that have been evaluated in sites of the African Trypanotolerant Livestock Network, using mainly N'Dama cattle. Results are discussed in the time sequence of the steps actually followed.
2. GENERAL RELATIONSHIPS BETWEEN TRYPANOSOMIASIS RISK AND CATTLE PERFORMANCE
The original large scale evaluation of the effect of trypanosomiasis risk (defined rather subjectively, but using all relevant information available to the researchers) on performance of N'Dama and West African Shorthorn cattle at 30 different sites, is shown in Table 1 (ILCA/FAO/UNEP, 1979).
| Trypanosomiasis risk | No. of sites | Calving (%) | Calf viability (%) | Calf weight (kg) | Cow weight (kg) | Productivity index (Kg)* | |
| \cow | \100 kg cow | ||||||
| Zero | 3 | 92.4a | 81.5 | 97.7 | 216 | 89.8a | 40.1a |
| Low | 13 | 73.1b | 84.6 | 98.1 | 212 | 68.2b | 31.9b |
| Medium | 10 | 54.8c | 79.7 | 96.7 | 200 | 47.2c | 23.2c |
| High | 4 | 56.1 | 67.8 | 93.1 | 192 | 29.6d | 18.8c |
Zero risk was confounded with intensive feeding and management, thus only low, medium and high risk could be directly compared. When performance levels under medium trypanosomiasis risk were compared with these achieved under low risk, calving percentage was 18% lower, calf viability 5% lower and calf weight 1% lower, resulting in a 30% lower productivity index per cow, and a 27% lower productivity per 100 kg of cow maintained per year. Similarly, when productivity levels under high risk were compared with those under low risk, calving percentage was 17% lower, calf viability 17% lower and calf weight 5% lower, resulting in a 56% lower productivity index per cow and a 41% lower productivity index per 100 kg of cow maintained per year. These results clearly showed that more accurate evaluation of the links between factors related to trypanosome infection and animal performance was essential.
3. SPECIFIC RELATIONSHIPS BETWEEN CRITERIA OF TRYPANOTOLERANCE AND CATTLE PERFORMANCE
At Mushie Ranch, Zaire, calving interval records were built up from N'Dama cows maintained for 3.5 years under a high natural tsetse-trypanosomiasis challenge. Monthly blood samples were examined by the buffy coat method to detect the presence of trypanosomes. The species of trypanosome was identified and the intensity of infection quantified as a parasitaemia score. The degree of anaemia was quantified by measuring packed red cell volume percent (PCV). Attempts were made to control other possible causes of anaemia; ticks by weekly dipping and internal parasites through a pasture management system involving extensive grazing conditions, no night paddocks, and regular burning of pastures (Trail et al., 1991b).
Trypanotolerance criteria and cow productivity
The comparative influences of time detected parasitaemic, parasitaemia intensity representing control of development of parasitaemia, and PCV value representing control of development of anaemia were measured on calving interval, calf weaning weight and cow productivity (weight of weaner calf per cow per annum) using least squares mixed model procedures.
| Criteria | Calving interval | Calf weaning weight | Cow productivity | |||
| days | % | kg | % | kg | % | |
| Low versus high time detected parasitaemic | -68 | -14.2 | 2.8 | 2.1 | 17.1 | 155 |
| Low versus high parasitaemia score (within high time detected parasitaemic) | -20 | -4.1 | 3.2 | 2.4 | 5.6 | 52 |
| High versus low PCV (within low time detected parasitaemic) | -27 | -6.3 | 7.8 | 5.8 | 12.6 | 104 |
| High versus low PCV (within high time detected parasitaemic) | -59 | -11.5 | 12.2 | 9.4 | 23.7 | 241 |
Results are summarised in Table 2 and significant findings included cows detected parasitaemic for a low length of time having a 14% shorter calving interval and a 15% higher productivity than their contemporaries that were parasitaemic for a high length of time. The effects of parasitaemia intensity were not significant. In contrast, animals maintaining a high PCV value had an 11% shorter calving interval a 9% heavier calf weaning weight; and a 24% superior cow productivity over those maintaining a low PCV value. So, control of development of anaemia, as measured by average PCV value, appeared to be the criterion of trypanotolerance most closely linked to overall cow productivity, in this production system where attempts had been made to control systematically other possible causes of anaemia.
Repeatabilities of trypanotolerance and performance traits
| Trait | Repeatabilities | ± S.E. |
| Time detected parasitaemic | 0.23±0.107 | |
| Parasitaemia score | 0 | |
| Average PCV | 0.33 ± 0.101 | |
| Calving interval | 0.20 ± 0.108 | |
| Calf weaning weight | 0.35 ± 0.100 | |
| Cow productivity | 0.10±0.109 |
Repeatabilities, between calving intervals, for the three trypanotolerance criteria and the three performance measures, all expressed as traits of the cow, were computed (Table 3). Traits with significant repeatabilities were calf weaning weight (0.35), average PCV over the calving interval (0.33) and time detected parasitaemic during the calving interval (0.23). The repeatability of PCV value was reasonably high and almost equal to that of calf weaning weight. Thus the ability to control development of anaemia, as indicated by PCV value, might well be a useful criterion of trypanotolerance with which to identify more trypanotolerant individual animals.
Assessment of trypanotolerance criteria in young animals
Simultaneous evaluation of the relative effects of criteria of trypanotolerance, in both the preweaner calf and its dam, on calf performance (weaning weight) showed that calf PCV values were at least as important as dam PCV values. Thus evaluation of criteria of trypanotolerance in an animal might be feasible before it reached maturity, but would need to be sufficiently long after weaning for the preweaning influence of the dam to have disappeared.
4. A FIELD TEST FOR TRYPANOTOLERANCE IN YOUNG N'DAMA CATTLE
The Zaire study suggested that investigations into practical field tests for trypanotolerance should focus on the use of post-weaners, maintained for varying lengths of time in as high natural tsetse-trypanosomiasis challenge situations as possible. Three such tests were carried out in which a total of 436 one-year-old N'Dama cattle were maintained for 12, 18 and 24 weeks under a medium tsetse-trypanosomiasis challenge at the Government Ranch (OGAPROV) in Gabon (Trail et al., 1991a).
Every 4 weeks in the first and every 2 weeks in the second and third tests, blood samples were examined by the buffy coat method to measure infection criteria. The degree of anaemia was estimated by measuring the PCV. Attempts were made to control other possible causes of anaemia. On the last day of the first and second tests, all animals were treated with Samorin (isometamidium chloride) at the rate of 1.0 mg/kg bodyweight by intramuscular injection, to evaluate the recovery of PCV values.
Trypanotolerance criteria and animal growth
The comparative sizes of the influence of parasitaemia control and anaemia control on N'Dama daily liveweight gain are summarized in Table 4. Ability to control the development of anaemia had a major effect on daily weight gain, four times that of the ability to control parasitaemia. Above average PCV values, as a measure of anaemia control, resulted in a 44% superior daily weight gain over below-average PCV values.
| Test number | Statistic | Parasitaemia controla | Anaemia controla | ||
| High score | Low score | High PCV | Low PCV | ||
| 1. | Animal number | 57 | 57 | 58 | 56 |
| Growth (g/day) | 248 | 273 | 283 | 238 | |
| S.E. | 23.5 | 23.9 | 21.0 | 206 | |
| 2. | Animal numbers | 51 | 51 | 46 | 56 |
| Growth (g/day) | 97 | 106 | 135 | 68 | |
| S.E. | 14.4 | 11.0 | 27.2 | 263 | |
| 3. | Animal numbers | 27 | 49 | 40 | 36 |
| Growth (g/day) | 81 | 89 | 111 | 59 | |
| S.E. | 19.0 | 19.1 | 23.2 | 259 | |
| Total | Animal numbers | 135 | 157 | 144 | 148 |
| Growth (g/day) | 142 | 156 | 176 | 122 | |
| S.E. | 19.0 | 19.1 | 23.1 | 259 | |
| Mean difference in growth (%) | +10 | +44 | |||
a Constructed from least squares means for classes within all periods when detected as parasitaemic.
Post-test recovery, of PCV values after trypanocidal drug treatment
| Percentage of treatment time detected parasitaemic | PCV at treatment (%) | PCV 30 days after (%) | ||
| Mean | c.v.a | Mean | c.v.a | |
| 0 | 33.1 | 15.9 | 36.5 | 8.7 |
| 25 | 26.7 | 18.7 | 34.8 | 8.7 |
| 50 | 22.1 | 22.8 | 33.0 | 8.8 |
| 80 | 18.8 | 26.5 | 34.0 | 8.7 |
At the completion of the first test, trypanosome prevalence was 30%, and the PCV values of groups that had been detected parasitaemic for varying percentages of the 12 week test period ranged from 33.1% for those never detected as parasitaemic, to 18.8% for those parasitaemic for 80% of the period. Coefficients of variation, indicating the amount of variation in PCV values within each group, ranged from 15,9% in animals never detected as parasitaemic to 26.5% in animals parasitaemic for 80% of the test period. On the last day of the test, all animals were treated with Samorin at the rate of the 1 mg/kg. When PCVs were measured 30 days later, major recovery of PCV had taken place, even those parasitaemic for 80% of the test period had a PCV value of 34%, and the coefficients of variation within all groups were reduced to 8.7%. In the second test, 73% of the recovery achieved one month after the trypanocidal drug treatment, had been reached in 9 days.
5. GENETIC ASPECTS OF CONTROL OF ANAEMIA DEVELOPMENT
Blood typing for parentage determination allowed genetic parameters of measures of control of anaemia to be evaluated (Trail et al., 1991c).
| Growth | Average PCV | Lowest PCV reached | |
| (a) Parasitaemia detection and parasitaemia score not included in analysis | |||
Growth | 0.22 ± 0.28 | 0.41 ± 0.73 | 0.13 ± 0.74 |
Average PCV | 0.35 | 0.35 ± 0.30 | 0.96 ± 0.20 |
Lowest PCV reached | 0.29 | 0.72 | 0.48 ± 0.31 |
| (b) Parasitaemia detection included in analysis | |||
Growth | 0.39 ± 0.30 | 0.71 ± 0.42 | 0.28 ± 0.55 |
Average PCV | 0.32 | 0.63 ± 0.33 | 0.99 ± 0.17 |
Lowest PCV reached | 0.25 | 0.66 | 0.51 ± 0.32 |
| (c) Parasitaemia detection and parasitaemic score included in analysis | |||
Growth | 0.39 ± 0.31 | 0.70 ± 0.42 | 0.28 ± 0.55 |
Average PCV | 0.32 | 0.64 ± 0.33 | 1.00 ± 0.17 |
Lowest PCV reached | 0.25 | 0.67 | 0.50 ± 0.32 |
Heritability is value on diagonal
Genetic correlation is value above diagonal
Phenotypic correlation is value below diagonal.
The heritabilities of, and genetic phenotypic correlations between growth, average PCV and lowest PCV reached on test are shown in Table 6. The heritability of body weight at the start of the test when animals averaged 50 weeks of age was 0.49 ± 0.32. This is within the normally reported range for this trait, while the large standard error could be a reflection of the small number of five progeny available per sire. When all environmental and parasitaemia information was taken into account, the heritability of growth over the test period was 0.39 ± 0,32, again within the expected range for growth over a 3 month period. The heritabilities of both PCV measures were higher than the corresponding heritability of growth being 0.64 ± 0.33 for average PCV and 0.50 ± 0.32 for lowest PCV reached.
The genetic correlation between average PCV and growth was 0.70 ± 0.42 and between lowest PCV reached and growth, 0.28 ± 0.55. These values, coupled with the higher heritabilities of the PCV measures, indicate some possibility of selection on PCV values for control of anaemia development.
6. TRYPANOSOME INFECTION DATA OVER COWS REPRODUCTIVE LIFETIME
First data on trypanosome infection detected by the buffy coat technique over cows reproductive lifetimes are becoming available (N. Wissocq, personal communication). At Mushie Ranch, Zaire, data from 186 N'Dama cows have been recorded monthly over an average of 5 years (range 3–7 years) under an average monthly trypanosome prevalence of 10%.
| Statistic | Mean ± S.E. | |
| Percentage of cows infected in 5 year reproductive lifetime | 95.7 | |
| Number of infections per cow | 5.5 ± 0.32 | |
| T. vivax : T. congolense infection ratio | 1.0 : 3.0 | |
| T. vivax : T. congolense infection ratio in calves | 1.0 : 0.9 | |
| Regression of average PCV% on number of infections detected | -1.3 ± 0.15 | |
| Least squares means for trypanosome species effect on average PCV% | ||
| T. vivax | 31.8 ± 0.15 | |
| T. congolense | 28.6 ± 0.47 | |
| Mixed T. vivax/T. congolense | 28.9 ± 0.93 | |
Table 7 shows that under this challenge level in Zaire, all N'Dama cows would be expected to be infected during their reproductive lifetime. Other findings noted in previous short term studies are confirmed, namely the major difference in T. vivax : T. congolense infection ratios between young calves and their dams grazing together, the effect of the number of infections per unit of time and the average PCV; and the different effects of species of trypanosomes infection on average PCV.
Accurate trypanosome species identification in detected infections is thus essential if clarification of linkages between infection, anaemia and animal performance is to be achieved.
7. ANTIGEN-DETECTION TEST FOR MORE ACCURATE MEASUREMENT OF TRYPANOSOME INFECTION.
So, in an attempt to measure infection more precisely, antigen-detection enzyme immunoassays developed by Nantulya at ILRAD were used for the diagnosis of Trypanosoma vivax, T. congolense and T. brucei in the same group of N'Dama cattle in Gabon (Trail et al., in press). The assays are based on monoclonal antibodies which recognise trypanosome antigens specific for each of the three species.
Buffy coat antigen test results
| Parasitaemia status | Antigenaemia status | Animals | |
| Number | % | ||
| Positive | Positive | 38 | 90 |
| Positive | Negative | 4 | 10 |
| 42 | |||
| Negative | Positive | 43 | 40 |
| Negative | Negative | 63 | 60 |
| 106 | |||
An average of 6 assays per animal were carried out over a 92 day period. Of the animals detected parasitaemic by the buffy coat technique, 90% were positive to the antigen test (table 8). More importantly, 40% of the animals with negative parasitological findings were also found to be antigen positive.
The proportion of animals with mixed species infections (T. congolense and T. vivax) over the 6 occasions when each animal was antigen-tested was 27% higher than the 17% found by the buffy coat technique. Additionally, on an individual sample basis, while it was extremely rare for a buffy coat examination to reveal a mixed species infection, 13% of all individual antigen tests did. It is possible that the difference reflects relative sensitivities of the two methods.
Genetic aspects of parasite control
When antigen positive, parasite negative animals were classified as having more ability to control parasite growth than parasitaemic animals, a significant sire effect suggested some possibility of a degree of genetic control being involved (Table 9). Thus the ELISA might offer a practical possibility for selection of trypanotolerant animals based on infection criteria.
| h2 ± S.E. | |
| Daily weight gain | 0.33 ± 0.47 |
| Lowest PCV reached | 0.45 ± 0.48 |
| Average PCV | 0.57 ± 0.49 |
| Parasite control | 1.08 ± 0.50 |
8. ANTIGEN-ELISA AND EFFICIENCY OF SELECTION OF N'DAMA CATTLE
Further work was then set up to more accurately evaluate relationships between trypanosome infection as measured by antigen detection enzyme immunoassays (antigen ELISA), anaemia as determined by average packed red cell volume (PCV), and animal performance as assessed by daily weight gain. 99 N'Dama cattle in Gabon were exposed to natural tsetse challenge at 11.5 months of age and recorded 14 times over a 13-week period (Trail et al., submitted).
Prevalence of mixed species infection
Approximately half the animals were found by the antigen test to be infected for an average of 5 of the 14 times that they were examined> 38% with Trypanosome congolense, 13% with T. vivax and 49% with a mixed infection. In individual samples, 14% had mixed species infections.
Effects of T. vivax and T. congolense infections on animal growth
T. congolense infections had significant deleterious effects on animal growth, while T. vivax infections did not. In animals with mixed infections, the regression of daily weight gain on the number of T. vivax infections in the mixed infection was -1.0 ± 3.3 g/day, while the regression of the gain on the number of T. congolense infections in the mixed infection was -6.2 ± 2.9 g/day. When the species effect was ignored, the overall regression of gain on the total number of infections was ignored, the overall regression of gain on the total number of infections was -3.6 ± 2.1 g/day. This shows again the importance of accurate trypanosome species identification in this region of Central Africa. A number of aspects previously reported were confirmed. Animals fund, on several repeated occasions, to be infected with T. congolense has significantly lower PCV values than those demonstrated to be infected on fewer occasions. Animals capable of maintaining PCV values, even when antigen ELISA positive on a high number of occasions, grew at the same rate as uninfected animals. Animals could not maintain PCV values when infected has poorer growth.
Antigen ELISA has the potential to increase the efficiency of selection of trypanotolerant N'Dama cattle under tsetse challenge in the field, in three main ways. Accurate identification of trypanosome species, especially in mixed species infections, clarifies linkages between infection, anaemia and animal performance. Detection of animals antigenaemic without patent parasitaemia could allow individuals with superior ability to control trypanosome infection to be identified. More accurate measurement of the proportion of time an animal is infected allows more accurate evaluation of its anaemia control capability.
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